Advances in stem cell proteomics

Current Opinion in Genetics and Development

Volumn 46, Issue , 2017, Pages 149-155

  Abazova, Nade ^a,b,c   Krijgsveld, Jeroen ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; HISTONE;

CELL PLASTICITY; CHROMATIN; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEOMICS; REVIEW; STEM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MASS SPECTROMETRY; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOMICS; STEM CELLS;

EID: 85030212556     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2017.07.007     Document Type: Review

References (73)

1. Nichols, J., Smith, A., Naive and primed pluripotent states. Cell Stem Cell 4 (2009), 487–492.
2. Wu, S.M., Hochedlinger, K., Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol 13 (2011), 497–505.
3. Inoue, H., Nagata, N., Kurokawa, H., Yamanaka, S., iPS cells: a game changer for future medicine. EMBO J 33 (2014), 409–417.
4. Holland, A., Ohlendieck, K., Comparative profiling of the sperm proteome. Proteomics 15 (2015), 632–648.
5. Mulvey, C.M., Schröter, C., Gatto, L., Dikicioglu, D., Fidaner, I.B., Christoforou, A., Deery, M.J., Cho, L.T.Y., Niakan, K.K., Martinez-Arias, A., et al. Dynamic proteomic profiling of extra-embryonic endoderm differentiation in mouse embryonic stem cells. Stem Cells 33 (2015), 2712–2725.
6. Shoemaker, L.D., Kornblum, H.I., Neural stem cells (NSCs) and proteomics. Mol Cell Proteomics 15 (2016), 344–354.
7. Benevento, M., Munoz, J., Role of mass spectrometry-based proteomics in the study of cellular reprogramming and induced pluripotent stem cells. Expert Rev Proteomics 9 (2012), 379–399.
8. Benevento, M., Tonge, P.D., Puri, M.C., Hussein, S.M.I., Cloonan, N., Wood, D.L., Grimmond, S.M., Nagy, A., Munoz, J., Heck, A.J.R., et al. Proteome adaptation in cell reprogramming proceeds via distinct transcriptional networks. Nat Commun, 5, 2014, 5613.
9. Hansson, J., Rafiee, M.R., Reiland, S., Polo, J.M., Gehring, J., Okawa, S., Huber, W., Hochedlinger, K., Krijgsveld, J., Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency. Cell Rep 2 (2012), 1579–1592.
10. Taleahmad, S., Mirzaei, M., Parker, L.M., Hassani, S.-N., Mollamohammadi, S., Sharifi-Zarchi, A., Haynes, P.A., Baharvand, H., Salekdeh, G.H., Proteome analysis of ground state pluripotency. Sci Rep, 5, 2015, 17985.
11. Song, J., Saha, S., Gokulrangan, G., Tesar, P.J., Ewing, R.M., DNA and chromatin modification networks distinguish stem cell pluripotent ground states. Mol Cell Proteomics 11 (2012), 1036–1047.
12. Boland, M.J., Nazor, K.L., Loring, J.F., Epigenetic regulation of pluripotency and differentiation. Circ Res 115 (2014), 311–324.
13. Muñ Oz, J., Stange, D.E., Schepers, A.G., Van De Wetering, M., Koo, B.-K., Itzkovitz, S., Volckmann, R., Kung, K.S., Koster, J., Radulescu, S., et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent “+4” cell markers. EMBO J 31 (2012), 3079–3091.
14. Klimmeck, D., Hansson, J., Raffel, S., Vakhrushev, S.Y., Trumpp, A., Krijgsveld, J., Proteomic cornerstones of hematopoietic stem cell differentiation: distinct signatures of multipotent progenitors and myeloid committed cells. Mol Cell Proteomics 11 (2012), 286–302.
15. Cabezas-Wallscheid, N., Klimmeck, D., Hansson, J., Lipka, D.B., Reyes, A., Wang, Q., Weichenhan, D., Lier, A., von Paleske, L., Renders, S., et al. Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis. Cell Stem Cell 15 (2014), 507–522.
16. Haas, S., Hansson, J., Klimmeck, D., Loeffler, D., Velten, L., Uckelmann, H., Wurzer, S., Prendergast Á.M., Schnell, A., Hexel, K., et al. Inflammation-induced emergency megakaryopoiesis driven by hematopoietic stem cell-like megakaryocyte progenitors. Cell Stem Cell 17 (2015), 422–434 Identification of a post-transcriptional mechanism imposing a megakaryocyte profile in activated hematopoietic stem cells in vivo.
17. Sun, B., Proteomics and glycoproteomics of pluripotent stem-cell surface proteins. Proteomics 15 (2015), 1152–1163.
18. Van Hoof, D., Dormeyer, W., Braam, S.R., Passier, R., Monshouwer-Kloots, J., Ward-van Oostwaard, D., Heck, A.J.R., Krijgsveld, J., Mummery, C.L., Identification of cell surface proteins for antibody-based selection of human embryonic stem cell-derived cardiomyocytes. J Proteome Res 9 (2010), 1610–1618.
19. Hao, J., Li, W., Dan, J., Ye, X., Wang, F., Zeng, X., Wang, L., Wang, H., Cheng, Y., Liu, L., et al. Reprogramming- and pluripotency-associated membrane proteins in mouse stem cells revealed by label-free quantitative proteomics. J Proteomics 86 (2013), 70–84.
20. Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., Watts, J.D., Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 27 (2009), 378–386.
21. Rugg-Gunn, P.J., Cox, B.J., Lanner, F., Sharma, P., Ignatchenko, V., McDonald, A.C.H., Garner, J., Gramolini, A.O., Rossant, J., Kislinger, T., Cell-surface proteomics identifies lineage-specific markers of embryo-derived stem cells. Dev Cell 22 (2012), 887–901.
22. Mallanna, S.K., Waas, M., Duncan, S.A., Gundry, R.L., N-glycoprotein surfaceome of human induced pluripotent stem cell derived hepatic endoderm. Proteomics, 2016, 10.1002/pmic.201600397.
23. Mallanna, S.K., Cayo, M.A., Twaroski, K., Gundry, R.L., Duncan, S.A., Mapping the cell-surface N-glycoproteome of human hepatocytes reveals markers for selecting a homogeneous population of iPSC-derived hepatocytes. Stem Cell Rep 7 (2016), 543–556.
24. Boheler, K.R., Bhattacharya, S., Kropp, E.M., Chuppa, S., Riordon, D.R., Bausch-Fluck, D., Burridge, P.W., Wu, J.C., Wersto, R.P., Chan, G.C.F., et al. A human pluripotent stem cell surface N-glycoproteome resource reveals markers, extracellular epitopes, and drug targets. Stem Cell Rep 3 (2014), 185–203.
25. Billing, A.M., Ben Hamidane, H., Dib, S.S., Cotton, R.J., Bhagwat, A.M., Kumar, P., Hayat, S., Yousri, N.A., Goswami, N., Suhre, K., et al. Comprehensive transcriptomic and proteomic characterization of human mesenchymal stem cells reveals source specific cellular markers. Sci Rep, 6, 2016, 21507.
26. Huang, X., Wang, J., The extended pluripotency protein interactome and its links to reprogramming. Curr Opin Genet Dev 28 (2014), 16–24.
27. Kwon, S.C., Yi, H., Eichelbaum, K., Föhr, S., Fischer, B., You, K.T., Castello, A., Krijgsveld, J., Hentze, M.W., Kim, V.N., The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 20 (2013), 1122–1130.
28. Do, E., kyoung, Cheon, H.C., Jang, I.H., Choi, E.J., Heo, S.C., Kang, K.T., Bae, K.H., Cho, Y.S., Seo, J.K., Yoon, J.H., et al. Reptin regulates pluripotency of embryonic stem cells and somatic cell reprogramming through Oct4-dependent mechanism. Stem Cells 32 (2014), 3126–3136.
29. Pardo, M., Lang, B., Yu, L., Prosser, H., Bradley, A., Babu, M.M., Choudhary, J., An expanded Oct4 interaction network: implications for stem cell biology, development, and disease. Cell Stem Cell 6 (2010), 382–395.
30. van den Berg, D.L.C., Snoek, T., Mullin, N.P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., Poot, R.A., An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6 (2010), 369–381.
31. Mallanna, S.K., Ormsbee, B.D., Iacovino, M., Gilmore, J.M., Cox, J.L., Kyba, M., Washburn, M.P., Rizzino, A., Proteomic analysis of Sox2-associated proteins during early stages of mouse embryonic stem cell differentiation identifies Sox21 as a novel regulator of stem cell fate. Stem Cells 28 (2010), 1715–1727.
32. Lai, Y.-S., Chang, C.-W., Pawlik, K.M., Zhou, D., Renfrow, M.B., Townes, T.M., SRY (sex determining region Y)-box2 (Sox2)/poly ADP-ribose polymerase 1 (Parp1) complexes regulate pluripotency. Proc Natl Acad Sci 109 (2012), 3772–3777.
33. Costa, Y., Ding, J., Theunissen, T.W., Faiola, F., Hore, T.A., Shliaha, P.V., Fidalgo, M., Saunders, A., Lawrence, M., Dietmann, S., et al. NANOG-dependent function of TET1 and TET2 in establishment of pluripotency. Nature 495 (2013), 370–374.
34. Gagliardi, A., Mullin, N.P., Ying Tan, Z., Colby, D., Kousa, A.I., Halbritter, F., Weiss, J.T., Felker, A., Bezstarosti, K., Favaro, R., et al. A direct physical interaction between Nanog and Sox2 regulates embryonic stem cell self-renewal. EMBO J 32 (2013), 2231–2247.
35. Oliviero, G., Brien, G.L., Waston, A., Streubel, G., Jerman, E., Andrews, D., Doyle, B., Munawar, N., Wynne, K., Crean, J., et al. Dynamic protein interactions of the Polycomb repressive complex 2 during differentiation of pluripotent cells. Mol Cell Proteomics 15 (2016), 3450–3460.
36. Kloet, S.L., Makowski, M.M., Baymaz, H.I., van Voorthuijsen, L., Karemaker, I.D., Santanach, A., Jansen, P.W.T.C., Di Croce, L., Vermeulen, M., The dynamic interactome and genomic targets of Polycomb complexes during stem-cell differentiation. Nat Struct Mol Biol 23 (2016), 682–690 Demonstration of dynamic composition of the PRC2 complex dependent on the stem cell state.
37. Vermeulen, M., Eberl, H.C., Matarese, F., Marks, H., Denissov, S., Butter, F., Lee, K.K., Olsen, J.V., Hyman, A.A., Stunnenberg, H.G., et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142 (2010), 967–980.
38. Eberl, H.C., Spruijt, C.G., Kelstrup, C.D., Vermeulen, M., Mann, M., A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol Cell 49 (2013), 368–378.
39. Spruijt, C.G., Gnerlich, F., Smits, A.H., Pfaffeneder, T., Jansen, P.W.T.C., Bauer, C., Münzel, M., Wagner, M., Müller, M., Khan, F., et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152 (2013), 1146–1159.
40. Engelen, E., Brandsma, J.H., Moen, M.J., Signorile, L., Dekkers, D.H.W., Demmers, J., Kockx, C.E.M., Ozgür, Z., van IJcken, W.F.J., van den Berg, D.L.C., et al. Proteins that bind regulatory regions identified by histone modification chromatin immunoprecipitations and mass spectrometry. Nat Commun, 6, 2015, 7155 Identification of proteins that specifically interact with modified histones representing enhancers, promoters and heterochromatin.
41. Rafiee, M.R., Girardot, C., Sigismondo, G., Krijgsveld, J., Expanding the circuitry of pluripotency by selective isolation of chromatin-associated proteins. Mol Cell 64 (2016), 624–635 Combination of ChIP with enrichment of biotinylated DNA to identify chromatin-bound protein networks.
42. Castello, A., Horos, R., Strein, C., Fischer, B., Eichelbaum, K., Steinmetz, L.M., Krijgsveld, J., Hentze, M.W., System-wide identification of RNA-binding proteins by interactome capture. Nat Protoc 8 (2013), 491–500.
43. Brimacombe, R., Stiege, W., Kyriatsoulis, A., Maly, P., Intra-RNA and RNA–protein cross-linking techniques in Escherichia coli ribosomes. Methods Enzymol 164 (1988), 287–309.
44. He, C., Sidoli, S., Warneford-Thomson, R., Tatomer, D.C., Wilusz, J.E., Garcia, B.A., Bonasio, R., High-resolution mapping of RNA-binding regions in the nuclear proteome of embryonic stem cells. Mol Cell 64 (2016), 416–430.
45. Sysoev, V.O., Fischer, B., Frese, C.K., Gupta, I., Krijgsveld, J., Hentze, M.W., Castello, A., Ephrussi, A., Global changes of the RNA-bound proteome during the maternal-to-zygotic transition in Drosophila. Nat Commun, 7, 2016, 12128.
46. Wessels, H.-H., Imami, K., Baltz, A.G., Kolinski, M., Beldovskaya, A., Selbach, M., Small, S., Ohler, U., Landthaler, M., The mRNA-bound proteome of the early fly embryo. Genome Res 26 (2016), 1000–1009.
47. Despic, V., Dejung, M., Gu, M., Krishnan, J., Zhang, J., Herzel, L., Straube, K., Gerstein, M.B., Butter, F., Neugebauer, K.M., Dynamic RNA–protein interactions underlie the zebrafish maternal-to-zygotic transition. Genome Res 27 (2017), 1184–1194.
48. Tadros, W., Lipshitz, H.D., The maternal-to-zygotic transition: a play in two acts. Development 136 (2009), 3033–3042.
49. Parker, C.E., Mocanu, V., Mocanu, M., Dicheva, N., Warren, M.R., Mass Spectrometry for post-translational modifications. 2010, CRC Press, Taylor & Francis.
50. Melo-Braga, M.N., Meyer, M., Zeng, X., Larsen, M.R., Characterization of human neural differentiation from pluripotent stem cells using proteomics/PTMomics-Current state-of-the-art and challenges. Proteomics 15 (2015), 656–674.
51. Brumbaugh, J., Russell, J.D., Yu, P., Westphall, M.S., Coon, J.J., Thomson, J.A., NANOG is multiply phosphorylated and directly modified by ERK2 and CDK1 in vitro. Stem Cell Rep 2 (2014), 18–25.
52. Brumbaugh, J., Hou, Z., Russell, J.D., Howden, S.E., Yu, P., Ledvina, A.R., Coon, J.J., Thomson, J.A., Phosphorylation regulates human OCT4. Proc Natl Acad Sci 109 (2012), 7162–7168.
53. Jeong, C.-H., Cho, Y.-Y., Kim, M.-O., Kim, S.-H., Cho, E.-J., Lee, S.-Y., Jeon, Y.-J., Yeong Lee, K., Yao, K., Keum, Y.-S., et al. Phosphorylation of Sox2 cooperates in reprogramming to pluripotent stem cells. Stem Cells 28 (2010), 2141–2150.
54. Piazzi, M., Williamson, A., Lee, C.-F., Pearson, S., Lacaud, G., Kouskoff, V., McCubrey, J.A., Cocco, L., Whetton, A.D., Quantitative phosphoproteome analysis of embryonic stem cell differentiation toward blood. Oncotarget 6 (2015), 10924–10939.
55. Singec, I., Crain, A.M., Hou, J., Tobe, B.T.D., Talantova, M., Winquist, A.A., Doctor, K.S., Choy, J., Huang, X., La Monaca, E., et al. Quantitative analysis of human pluripotency and neural specification by in-depth (phospho)proteomic profiling. Stem Cell Rep 7 (2016), 527–542 Very deep phospho-proteomic study uncovering multiple regulatory processes during neuronal differentiation.
56. 2 enrichment combined with 2D LC–MS/MS and pathway mapping. Proteomics 13 (2013), 1325–1333.
57. Wang, L.D., Ficarro, S.B., Hutchinson, J.N., Csepanyi-Komi, R., Nguyen, P.T., Wisniewski, E., Sullivan, J., Hofmann, O., Ligeti, E., Marto, J.A., et al. Phosphoproteomic profiling of mouse primary HSPCs reveals new regulators of HSPC mobilization. Blood 128 (2016), 1465–1474.
58. Phanstiel, D.H., Brumbaugh, J., Wenger, C.D., Tian, S., Probasco, M.D., Bailey, D.J., Swaney, D.L., Tervo, M.A., Bolin, J.M., Ruotti, V., et al. Proteomic and phosphoproteomic comparison of human ES and iPS cells. Nat Methods 8 (2011), 821–827.
59. Christophorou, M.A., Castelo-Branco, G., Halley-Stott, R.P., Oliveira, C.S., Loos, R., Radzisheuskaya, A., Mowen, K.A., Bertone, P., Silva, J.C.R., Zernicka-Goetz, M., et al. Citrullination regulates pluripotency and histone H1 binding to chromatin. Nature 507 (2014), 104–108.
60. Sridharan, R., Gonzales-Cope, M., Chronis, C., Bonora, G., Mckee, R., Huang, C., Patel, S., Lopez, D., Mishra, N., Pellegrini, M., et al. Proteomic and genomic approaches reveal critical functions of H3K9 methylation and heterochromatin protein-1gamma in reprogramming to pluripotency. Nat Cell Biol 15 (2013), 872–882.
61. Bhanu, N.V., Sidoli, S., Garcia, B.A., Histone modification profiling reveals differential signatures associated with human embryonic stem cell self-renewal and differentiation. Proteomics 16 (2016), 448–458.
62. Benevento, M., Tonge, P.D., Puri, M.C., Nagy, A., Heck, A.J.R., Munoz, J., Fluctuations in histone H4 isoforms during cellular reprogramming monitored by middle-down proteomics. Proteomics, 15,2015, 3219-3231., 10.1002/pmic.201500031.
63. Gonzales-Cope, M., Sidoli, S., Bhanu, N.V., Won, K.-J., Garcia, B.A., Histone H4 acetylation and the epigenetic reader Brd4 are critical regulators of pluripotency in embryonic stem cells. BMC Genomics, 17, 2016, 95.
64. Hughes, C.S., Foehr, S., Garfield, D.A., Furlong, E.E., Steinmetz, L.M., Krijgsveld, J., Ultrasensitive proteome analysis using paramagnetic bead technology. Mol Syst Biol, 10, 2014, 757.
65. Eichelbaum, K., Winter, M., Berriel Diaz, M., Herzig, S., Krijgsveld, J., Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat Biotechnol, 30,2012, 984-990., 10.1038/nbt.2356.
66. Eichelbaum, K., Krijgsveld, J., Rapid temporal dynamics of transcription, protein synthesis, and secretion during macrophage activation. Mol Cell Proteomics 13 (2014), 792–810.
67. Buszczak, M., Signer, R.A.J., Morrison, S.J., Cellular differences in protein synthesis regulate tissue homeostasis. Cell 159 (2014), 242–251.
68. Rees, J.S., Li, X.-W., Perrett, S., Lilley, K.S., Jackson, A.P., Protein neighbors and proximity proteomics. Mol Cell Proteomics 14 (2015), 2848–2856.
69. Christoforou, A., Mulvey, C.M., Breckels, L.M., Geladaki, A., Hurrell, T., Hayward, P.C., Naake, T., Gatto, L., Viner, R., Arias, A.M., et al. A draft map of the mouse pluripotent stem cell spatial proteome. Nat Commun, 7, 2016, 9992 Extensive sub-cellular fractionation gives insight in the spatial distribution of thousands of proteins across organelles and protein complexes in ES cells.
70. Klimmeck, D., Cabezas-Wallscheid, N., Reyes, A., von Paleske, L., Renders, S., Hansson, J., Krijgsveld, J., Huber, W., Trumpp, A., Transcriptome-wide profiling and posttranscriptional analysis of hematopoietic stem/progenitor cell differentiation toward myeloid commitment. Stem Cell Rep 3 (2014), 858–875.
71. Lechman, E.R., Gentner, B., Ng, S.W.K., Schoof, E.M., van Galen, P., Kennedy, J.A., Nucera, S., Ciceri, F., Kaufmann, K.B., Takayama, N., et al. miR-126 regulates distinct self-renewal outcomes in normal and malignant hematopoietic stem cells. Cancer Cell 29 (2016), 214–228.
72. Abraham, S.A., Hopcroft, L.E.M., Carrick, E., Drotar, M.E., Dunn, K., Williamson, A.J.K., Korfi, K., Baquero, P., Park, L.E., Scott, M.T., et al. Dual targeting of p53 and c-MYC selectively eliminates leukaemic stem cells. Nature 534 (2016), 341–346.
73. Cristobal, A., van den Toorn, H.W.P., van de Wetering, M., Clevers, H., Heck, A.J.R., Mohammed, S., Personalized proteome profiles of healthy and tumor human colon organoids reveal both individual diversity and basic features of colorectal cancer. Cell Rep 18 (2017), 263–274.